liver cirrhosis;nodul.txt

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TheBritishJournalofRadiology,78(2005), 355357 E2005 The British Institute of RadiologyDOI: 10.1259/bjr/36150185

Casereport

Thereversetargetsigninliverdisease:apotentialultrasound

featureincirrhoticlivernodulescharacterization

1GJKRAUS,MD,1P

SCHEDLBAUER,MD,2SLAX,MD,3DZEBEDIN,MDand1FFLUECKIGER,MD

Institutesof1Radiologyand2Pathology,GeneralHospitalGraz-West,Goestingerstrasse


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22,8020Grazand3

DepartmentofRadiology,UniversityHospitalGraz,Auenbruggerplatz1,8036Graz,Austria

Abstract.In patients with suspected liver disease, ultrasound is the most commonly performed initial imagingmodality. We report a patient who had previously undiagnosed liver cirrhosis with target-shaped lesions

interspersed throughout the liver parenchyma on ultrasound seen as multiple uniform round shaped lesions withvarying isoechoic to hyperechoic centres surrounded by a hyperechoic rim. We have termed this the reversetarget sign as there is inversion of the typical echoic pattern that is normallyseen in metastatic liver disease. Wesuggest this ultrasound sign may represent a method for differentiating cirrhotic liver nodules from other

nodular liver lesions.

Ultrasound is often the preliminary and most widelyavailable imaging modality in evaluation of liver disease.

The ultrasound and the CT appearance of metastatic liverdisease and cirrhotic nodules can be quite similar. If thereare no concomitant morphological imaging findings, thedifferential diagnosis is based on histology and clinicalhistory.

Casereport

A 55-year-old patient was referred to our institutionfor the liver ultrasound because of a weight loss of 17 kgover 3 months. His alanine aminotransferase (56 U l21;

normal range 522 U l21), aspartate aminotransferase(33 U l21; normal range 518 U l21), alkaline phosphatase(214 U l21, normal range 60170 U l21) andgamma glutamyle transferase (35 U l21; normal range528 U l21) were elevated, and his cholinesterase(1444 U l21; normal range 530012 920 U l21) wasbelow the reference value. All other laboratory valuesconcerning the liver were within the normal range.

The prior medical history revealed that the patient


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suffered from pulmonary tuberculosis, as well as noninsulin dependent diabetes mellitus. Serology for viralhepatitis A, B and C proved to be negative.

Ultrasound (Combison 401; General Electric MedicalSystems, Milwaukee, WI) showed multiple lesions dispersedthroughout the whole liver parenchyma with anisoechoic to hyperechoic centre and a hyperechoic rim(Figure 1). On colour Doppler ultrasound, there wasregular hepatopetal blood flow in the portal vein.

On a triple phase CT-scan the lesions were best visible inthe unenhanced phase (Figure 2), faintly visible as slightlyhypodense lesions in the portalvenous phase at 70 s delay(not shown) and isodense to liver parenchyma in a delayedphase at 180 s. In the unenhanced phase the large centrewas slightly hypodense to liver parenchyma imbedded in amore hypodense rim (Figure 2). There was delayed uptake

Received21June2004and

inrevisedform12November2004,accepted5January2005.

of contrast media in the centre and subtle enhancement

of the rim in the portalvenous phase (not shown).There was no nodularity of the liver contour and theratio of the caudate lobe to the right lobe was within thenormal range (i.e.,0.6). Secondary changes of cirrhosissuch as ascites, varicose venous collaterals and splenomegalywere absent.

The most likely diagnosis was of metastatic liver disease.We did not perform contrast-enhanced ultrasound orMRI.

For further diagnostic work-up biopsy under ultrasoundguidance was performed, and a 16 G SurecutTM biopsy

needle (Boston Scientific, Natick, MA) was used. Thehistological specimens of two representative lesionsshowed features of large regenerating nodules withchanges such as architectural distortion, cirrhosis andsteatosis of hepatocytes (Figure 3).

Figure1.Ultrasound (B-mode) shows disseminated isoechoic


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to hyperechoic macronodular lesions with a hyperechoic rim(reverse target sign) throughout the liver parenchyma.

TheBritishJournalofRadiology,April2005


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Figure2.On an unenhanced spiral CT-scan, the lesions areisodense to liver parenchyma with a hypoattenuating rim.

Discussion

Cirrhotic nodules and dysplastic nodules (DN), withdifferent grades of histological differentiation, are viewedas a spectrum of changes towards possible hepatocellularcarcinoma [1] with up to 21.5% of nodules in cirrhoticlivers proving to be dysplastic [2]. Cirrhotic or regenerativenodules (RN) and DN can show a variety ofultrasound and CT patterns [3]. Many malignant liverlesions may typically present a sonolucent halo, the socalled target sign or bulls-eye lesion [4]. The histomorphologicalaetiology of this sonolucent halo is controversialand has been correlated with an aggressive growthpattern, although it is non-specific and can also be seenin hepatocellular carcinoma, adenoma, focal nodular

Figure3.Histology: regenerative nodule with fibrocirrhoticchanges (white arrows) surrounding partly steatotic hepatocytes(black arrows) (Chronotrop-Aniline-Blue stain, magnification406).

GJKraus,PSchedlbauer,S

Laxetal

hyperplasia, haemangioma, lymphoma and fungal micro-abscesses [4].

However, in our patient, the rim was hyperechoic, whichis believed to correspond with a histological pattern ofseptal fibrosis and increased vascularity (Figure 3). Owingto this sonomorphological pattern, we have termed it thereverse target sign. The ultrasound patterns of metastatic

liver disease are variable, and correlated with thehistology of the primary tumour can be echogenic,hypoechoic, cystic, infiltrative, and may even calcify [4].Haemangiomas larger than 3 cm can also have thesonomorphological pattern of the reverse target sign andshould be considered in the differential diagnosis [5]. OnCT the typical nodular dynamic contrast enhancementwith filling-in centripetally is missing, the lesions aremore radio-opaque than haemangiomas, and haemangiomasdo not occur in the disseminated fashion seen in our


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patient.

The multiplicity of the lesions and missing signs ofcirrhosis, such as contour irregularity, led us to thehypothesis of metastatic liver disease. Surface nodularityof the liver has the highest diagnostic accuracy andspecificity for cirrhosis compared with caudate lobehypertrophy and hepatic venous blood flow patterns inultrasound [6], and it might have been useful to assess theliver surface, using a high frequency linear array probe.

The role of MRI in the diagnosis of nodular liver lesionsis still uncertain [3]. Ferumoxide-particles administeredintravenously are cleared by phagocytosis by Kupffer cells,and this shortens the T2* signal [7]. DN and RN have analmost identical or even increased number of Kupffer cellscompared with the surrounding parenchyma. Metastatictumours are devoid of Kupffer cells; therefore ferumoxideenhancedMRI can help to differentiate metastases fromRN. But moderately and poorly differentiated HCCdevelopment in a cirrhotic liver are also found to have asignificantly decreased number of Kupffer cells [8]. MRI ismore accurate in the detection of nodular liver lesion inthe cirrhotic liver than CT but tumour size is a restricting

factor and small lesions can easily be missed [9].

The characterization of focal liver lesions with Gd-BOPTA and dynamic contrast enhanced MRI may be ofgreater importance in the future [10].

In summary, the diagnostic work-up of nodular liverlesions in some patients, even using all radiodiagnosticmodalities, can be misleading and lead to misdiagnosis.Clinical and laboratory findings, as well as patient historymay help in achieving the correct diagnosis. Although liverbiopsy can yield false-negative results in about one-third ofpatients, for accurate characterization of liver nodules

biopsy and histology remains the gold standard [11].

References

1. InternationalWorking Party. Terminology of nodularhepatocellular lesions. Hepatology 1995;22:98393.2. TeradaT, Terasaki S, Nakanuma Y. A clinicopathologicstudy of adenomatous hyperplasia of the liver in 209consecutive cirrhotic livers examined by autopsy. Cancer1993;72:15516.

3. LimJH, Choi BJ. Dysplastic nodules in liver cirrhosis:imaging. Abdom Imaging 2002;27:1178.4. Harvey CJ, Albrecht T. Ultrasound of focal liver lesions. EurRadiol 2001;11:157893.TheBritishJournalofRadiology,


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April2005


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Casereport:Reversetargetsigninliverdisease

5. Leifer DM, Middleton WD, Teefey SA, Menias CO, LeahyJR. Follow-up of patients at low risk for hepatic malignancywith a characteristic hemangioma at US. Radiology2000;214:16772.6. Colli A, Fraquelli M, Andreoletti M, Marino B, Zuccoli E,Conte D. Severe liver fibrosis or cirrhosis: accuracy of US fordetection-analysis of 300 cases. Radiology 2003;227:8994.7. StarkDD, Weissleder R, Elizondo G, Hahn PF, Saini S,Todd LE, et al. Superparamagnetic iron oxide: clinicalapplication as a contrast agent for MR imaging of theliver. Radiology 1988;168:297301.8. Tanaka

M, Nakashima O, Wada Y, Kage M, Kojiro M.Pathomorphological study of Kupffer cells in hepatocellularcarcinoma and hyperplastic nodular lesions in the liver.Hepatology 1996;24:80712.9. de Ledinghen V, Laharie D, Lecesne R, Le Bail B, WinnockM, Bernard PH, et al. Detection of nodules in liver cirrhosis:spiral computed tomography or magnetic resonance imaging?A prospective study of 88 nodules in 34 patients. Eur JGastroenterol Hepatol 2002;14:15965.10. Schneider G, Grazioli L, Morana G, Kirchin M, Seidel R,Altmeyer K. Characterization of focal liver lesions with Gd-BOPTA: a review of imaging findings on unenhanced,dynamic, and hepatobiliary phase MR imaging. (Abstract)

RSNA 2003 URL: http://rsna2003.rsna.org/rsna2003/VBK/conference/event_display.cfm?em_id53106019 (cited 10December 2003).11. Poniachik J, Bernstein DE, Reddy KR, Jeffers LJ, Coelho-Little ME, Civantos F, et al. The role of laparoscopy in thediagnosis of cirrhosis. Gastrointest Endosc 1996;43:56871.TheBritishJournalofRadiology,April2005


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